The invasive avian vampire fly, Philornis downsi, Dodge and Aitken (Diptera: Muscidae) is a threat to the long‐term conservation of Darwin's finches and other landbirds in the Galapagos Islands. Adult flies feed on fermented fruit, but their larvae are obligate parasites that feed on, and often cause the mortality of, the developing nestlings. Various techniques for the control of this parasite are currently under study, but the inability to rear flies in captivity has slowed progress. To help understand the reproductive behaviour of P. downsi, in this study, we measured the reproductive organs of male and female flies to determine the age flies mature physiologically, as well as the influence of the larval and adult diets on this process. Both females and males reared from larvae that had developed in the wild on live birds reached physiological maturity at 6 days; in the males, this was associated with increased pigmentation of the testes and the presence of free sperm, and in the females, mature eggs. Females reared in the laboratory on an artificial diet produced mature eggs at 6 days. However, the ovaries of laboratory‐reared females were statistically smaller than those of wild females, suggesting that egg production was affected by larval diet. Physiological maturity was delayed in laboratory‐reared males, taking twice as long. The testes of these males had more unpigmented areas and deformities indicating that the artificial larval diet was insufficient. Enrichment of the adult diet could help compensate for this. The addition of methoprene (M) to the diet was found to have a positive effect on the sexual development of the flies. In females, a diet of sugar + yeast hydrolysate (YH) in a 3:1 ratio combined with M favoured the development of larger ovaries and the production of mature eggs at an earlier age (3 days). In the case of males, a diet with YH increased testis size and M accelerated the growth of testis length even when males were fed only with sugar and without YH. Additional studies are recommended for improving the diets for mass‐rearing this highly harmful fly.